Genome-wide circular RNAs signatures involved in sexual maturation and its heterosis in chicken

Abstract

Sexual maturation heterosis has been widely exploited in animal crossbreeding. However, the underlying mechanism has been rarely explored in chicken. In the present study, we performed the reciprocal crossing between White Leghorn and Beijing You chicken to evaluate the phenotypes related to sexual maturation, and profiled the ovary circRNAs of purebreds (WW, YY) and crossbreds (WY, YW) to elucidate the molecular mechanism underlying heterosis for sexual maturation. Pubic space and oviduct length exhibited positive heterosis, and age at first egg (AFE) exhibited negative heterosis in the crossbreds. We identified 3,025 known circRNAs and 624 putative circRNAs, which were mainly derived from the exons. Among these circRNAs, 141 and 178 circRNAs were specially expressed in WY and YW, respectively. There were 52.38% and 64.63% of total circRNAs in WY and YW exhibited non-additive expression pattern, respectively. GO enrichment and KEGG pathway analysis showed that the host genes of non-additive circRNAs were mainly involved in TGF-beta signaling pathway, oocyte development, ATPase activator activity, oocyte meiosis, progesterone-mediated oocyte maturation and GnRH signaling pathway. Weighted gene co-expression network analysis identified that four modules were significantly (P < 0.05) correlated with oviduct length and pubic space. The host genes of non-additive circRNAs harbored in the four modules were associated with MAPK signaling pathway and Wnt signaling pathway. Furthermore, competing endogenous RNAs (ceRNA) network analysis characterized non-additive circRNAs gal-FGFR2_0005 and gal-MAPKAP1_0004 could interact with gga-miR-1612 and gga-miR-12235-5p to regulate CNOT6, COL8A1, and FHL2, which were essential for ovary development, indicating that the non-additive circRNAs involved in the formation of sexual maturation heterosis through regulating genes related to the reproductive and developmental process. The findings would provide a deeper understanding of the molecular mechanism underlying sexual maturation heterosis from a novel perspective.